The Architecture of the Connective Tissue in the Musculoskeletal System

8/11/2019 The Architecture of the Connective Tissue in the Musculoskeletal System

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The Architecture of theConnective Tissue in the

Musculoskeletal SystemAnOften Overlooked FunctionalParameter as to Proprioceptionin the Locomotor Apparatus

Jaap van der al! M"! Ph"University Maastricht, Faculty of Health, Medicine and Life Sciences, Department of Anatomy and

Embryology, Maastricht, etherlands

Editor's Note: !his article is based on the doctoral thesis presented by the author at theUniversity Maastricht in "#$$% &!he 'rgani(ation of the Substrate of )roprioception in the Elbo*+egion of the +at &

The architecture of the connective tissue! includin# structures such as fasciae! sheaths!and mem$ranes! is more important for understandin# functional meanin# than is moretraditional anatomy! %hose anatomical dissection method ne#lects and denies thecontinuity of the connective tissue as inte#ratin# matri& of the $ody'

The connective tissue anatomy and architecture e&hi$its t%o functional tendencies thatare present in all areas of the $ody in different %ays and relationships' (n $ody cavities!the )disconnectin#) *uality of shapin# space ena$les mo$ility+ $et%een or#ans and $odyparts! the )connectin#) dimension ena$les functional mechanical interactions' (n themusculoskeletal system! those t%o features of the connective tissue are also present'They cannot $e found $y the usual analytic dissection procedures' An architecturaldescription is necessary'

This article uses such a methodolo#ic approach and #ives such a description for thelateral el$o% re#ion' The result is an alternative architectural vie% of the anatomicsu$strate involved in the transmission and conveyance of forces over synovial ,oints' Anarchitectural description of the muscular and connective tissue or#ani-ed in series %itheach other to ena$le the transmission of forces over these dynamic entities is more

appropriate than is the classical concept of )passive) force.#uidin# structures such asli#aments or#ani-ed in parallel to actively force.transmittin# structures such as muscles%ith tendons'

The discrimination $et%een so.called ,oint receptors and muscle receptors is anartificial distinction %hen function is considered' Mechanoreceptors! also the so.calledmuscle receptors! are arran#ed in the conte&t of force circumstancesthat is! of thearchitecture of muscle and connective tissue rather than of the classical anatomicstructures such as muscle! capsules! and li#aments' (n the lateral cu$ital re#ion of therat! a spectrum of mechanosensitive su$strate occurs at the transitional areas $et%eenre#ular dense connective tissue layers and the muscle fascicles or#ani-ed in series %iththem' This su$strate e&hi$its features of type and location of the mechanosensitivenerve terminals that usually are considered characteristic for ),oint receptors) as %ellas for )muscle receptors')

The receptors for proprioception are concentrated in those areas %here tensile stressesare conveyed over the el$o% ,oint' Structures cannot $e divided into either ,oint


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receptors or muscle receptors %hen muscular and colla#enous connective tissuestructures function in series to maintain ,oint inte#rity and sta$ility' (n vivo! thoseconnective tissue structures are strained durin# movements of the skeletal parts! thosemovements in turn $ein# induced and led $y tension in muscular tissue' (n principle!$ecause of the architecture! receptors can also $e stimulated $y chan#es in muscletension %ithout skeletal movement! or $y skeletal movement %ithout chan#e in muscletension' A mutual relationship e&ists $et%een structure /and function0 of the

mechanoreceptors and the architecture of the muscular and re#ular dense connectivetissue' 1oth are instrumental in the codin# of proprioceptive information to the centralnervous system'

KEYWORDS: Fascia, dissection, connective tissue, skeletal muscle, proprioception, elbow oint

PHILOSOPHIC AND METHODOLOGICINTRODUCTIONHow to Define Fasciae Anatomically in Gene!al an" in t#e M$sc$los%eletalSystem in Pa!tic$la!&

Some t!irt"#$ive "ears a%o, w!en & received m" $irst trainin% as anatomist, it was not customar" to$ocus one's met!odolo%ic attention on t!e anatom" o$ connective tissue in %eneral or o$ $asciae inparticular( On t!e contrar", one was more or less trained to consider $asciae to be connectivela"ers t!at !ad to be removed( )!is approac! is related to t!e $act t!at t!e proper met!od andprocedure o$ anatom" was and still is dissection(

*lt!ou%! dissection is no lon%er t!e main approac! in visuali+in% t!e anatom" and structure o$ t!e!uman bod" modern ima%in% tec!ni-ues can do so in t!e livin% bod" .dissectional t!inkin%. stillis t!e main met!od o$ anal"+in% t!e bod" in its anatom"( /ut in t!e da"s o$ m" trainin%, one !adto separate to .dissect. and t!e revealed structures !ad to be .cleaned. and .cleared. o$connective tissue( 0onnective tissue was somet!in% resemblin% a coverin% or sleeve over and

between t!e dissected structures( )!ere$ore it o$ten !ad to be removed durin% t!e dissectionprocedure(

1ost anatom" te2tbooks toda" s!ow muscles as discrete anatomic structures wit! t!e surroundin%and envelopin% connective tissue la"ers removed( W!en connective tissue was met as a la"er, amembrane, a $ascia coverin% a bod" structure, or%an, or re%ion, it was %iven a name derived $romt!e anatomic substrate t!at t!e la"er covered( 0onnective tissue anatom" is o$ten de$ined as asub#or%ani+ation o$ anatomic structures suc! as muscles, or%ans, and so on( Fasciae are t!usconsidered to be .part o$. or%ans and structures(

&n leadin% te2tbooks, $asciae are t!ere$ore de$ined as .masses o$ connective tissue lar%e enou%!to be visible wit! t!e unaided e"e. 34 5 3p( 675 and classi$ied as anatomic entities or structuresrelated to or%ans( /ut are $asciae, membranes, s!eat!s in t!e bod" in $act distinct and discreteanatomic structures, or are we dealin% wit! continuit"8 &s t!e anatomical view missin% somet!in%

w!en it allocates parts o$ t!is $ascial continuit" to anatomic structures and entities suc! as bod"walls or re%ions 3$or e2ample, $ascia endot!oracica or $ascia colli media5, or%ans 3$or e2ample,$ascia renalis5, or bod" parts 3$or e2ample, $ascia cruris58 &n addition, does a topo%rap!icperspective on $ascia %ive an" clue about t!e kind o$ arc!itectural, $unctional9mec!anicalrelations!ip bein% dealt wit!8

Sc!leip mentions t!e $ascia as .t!e dense irre%ular connective tissue t!at surrounds and connectsever" muscle, even t!e tiniest m"o$ibril, and ever" sin%le or%an o$ t!e bod" $ormin% continuit"t!rou%!out t!e bod"(. 37, 5 &n t!is wa", $ascia is considered an important inte%rative element in!uman posture and movement or%ani+ation 3locomotor apparatus5 and is o$ten re$erred to as t!e.or%an o$ $orm(. 36 5 Does an anal"tical and .dissectional. approac! to anatom" do ustice to t!isconcept8

&n removin% or dissectin% t!e connective tissue in t!e $orm o$ .la"ers,. ever" anatomist observes,

but o$ten overlooks, various de%rees o$ attac!ment( Sometimes a la"er o$ $ascia is ust loosel"connected wit! t!e underl"in% or nei%!borin% structure or tissue; sometimes, it is ver" ti%!t andinterwoven wit! it, and t!e $ascia reall" !as to be cut awa", as is t!e case wit! t!e $ascia cruris,
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$or e2ample( &n bot! cases, t!e concept o$ .dissected means discrete. tends to remain, wit! $asciaviewed as distinct $rom ot!er tissues, e2cept $or t!ose clearl" or%ani+ed in a mec!anical in-series relations!ip wit! muscular tissue, as in reco%ni+ed au2iliar" structures suc! as tendons andaponeuroses(

)!is met!odolo%ic mentalit" !as also lead traditional anatom" to dissect t!e musculoskeletals"stem into discrete anatomic structures as represented b" bones, oints, and muscles( )!epresent article s!ows t!at arc!itectural and mec!anical spatial relations!ips between t!e varioustissue components o$ t!e musculoskeletal s"stem reveal $unctional units t!at %o across t!etraditional anatomic entities o$ bones, oints, and muscles(

)!is lar%er view o$ functional relations!ips and co!erence is supported b" modernneurop!"siolo%"( &n t!e central nervous s"stem, t!e traditional anatomic or%ani+ation o$ t!emusculoskeletal s"stem is onl" ver" poorl" represented topolo%icall", i$ at all( )!e $unctional andcoordinated components o$ position and motion are not t!e muscles 3and oints5, but movementsand per$ormed actions( 1odern task#dependent models as initiated b" 5 indicate t!at motorunits are not necessaril" or%ani+ed in t!e central nervous s"stem wit! respect to individual motornuclei, but accordin% to be!avioral tasks( )!is or%ani+ation su%%ests t!at !umans conceptuali+e alocomotion s"stem in a $roader sense , includin% t!e coordinatin% and re%ulatin% nervous s"stem3central as well as perip!eral5, and discriminate t!at $rom t!e locomotion s"stem in t!e narro%ersense 3locomotor apparatus5, w!ic! is represented b" t!e actual musculoskeletal s"stem(

Contin$ity an" Connecti'ity(Connecti'e Tiss$e as Mat!i)

?nder t!e procedural and mental scalpel o$ t!e anatomist, t!e continuit" o$ t!e connective tissueas central matri2 o$ t!e bod" !as been lost( )!e primar" connective tissue o$ t!e bod" is t!eembr"onic mesoderm( )!e mesoderm represents t!e matri2 and environment wit!in w!ic! t!eor%ans and structures o$ t!e bod" !ave been di$$erentiated and t!ere$ore are embedded( )!e@erman embr"olo%ist /lec!sc!midt t!ere$ore distin%uis!ed t!e mesoderm as %erminal la"er: an.inner tissue. in opposition to t!e ectoderm and endoderm as .limitin% tissues(. &n !istolo%",.limitin% tissue. is commonl" called epit!elium and is constituted almost solel" o$ cells, wit!relativel" little intercellular space( .&nner tissue. could be described as undi$$erentiated connectivetissue, mesenchyme, and is in principle or%ani+ed in t!ree components: cells, intercellular space3interstitial substances5, and $ibers( 3A,B5 1ost derivatives o$ t!e so#called inner tissue can beidenti$ied in !istolo%" as connective tissue, includin% t!e !ead#mesenc!"me as derivative $romneurodermal tissue(

*s to t!e functional development and di$$erentiation o$ t!e mesenc!"me, t!ere are two patternso$ .connection(.

)!e $irst pattern is t!e development o$ .intercellular space,. w!ic! represents a $issure $unctionin%as a slidin% and slippin% space as is seen in t!e $ormation o$ coelom 3bod" cavities5 and o$ oint.cavities(. &n t!is pattern, spatial separation is ensured and t!ere$ore motion is enabled( &n suc!cavit" $ormation processes, t!e primar" enlar%ed intercellular space is lined up and delimited b"an epit!elium 3in bod" cavities, a so#called mesot!elium5( Suc! epit!elia more or less depend ont!e presence o$ continuous motion $or t!eir $unctional maintenance( Fascial la"ers suc! asperitoneum and pleural membrane tend to ad!ere as soon as t!e movement o$ t!e relatedstructures and or%ans becomes absent( )!is p!enomenon can also be observed in immobili+ed

oints, s!owin% t!at, in $unctional perspective, bod" cavities and oint spaces !ave similarities(

)!e second pattern o$ development and di$$erentiation o$ t!e mesenc!"me is t!e $ormation o$ abindin% medium, eit!er $ibers 3as in re%ular dense connective tissue structures suc! asmembranes and li%aments5 or interstitial substrate and matri2 3$or e2ample, con$i%ured incartila%inous oints5( )!is pattern represents t!e $unctional tendenc" o$ .connectin%. b" means o$t!e tissue components o$ t!e mesenc!"me 3one or a combination o$ cells, intercellular substance,and $ibers5(

&n suc! a wa", a w!ole spectrum o$ connectivit" could be described in t!e musculoskeletal s"stem(On t!e one e2treme, connectin% structures resemble t!e desmal sutures in t!e skull, w!ere denseconnective tissue membranes indeed construct a nearl" immobile oint connection( )!e ot!ere2treme is represented b" t!e s"novial oints 3articulations5, w!ere t!e uttermost mobilit" ise2erted( )!is latter con$i%uration is also s!own in t!e $issures o$ t!e bod" cavities, w!ere or%ansand bod" walls and or%ans t!emselves are .connected. in a relations!ip o$ mobilit"( )!ecartila%inous oints 3s"mp!"ses5 more or less represent an intermediate scale o$ connectin%: in!umans, nearl" all t!e classical s"mp!"ses 3suc! as t!e ones between t!e vertebrae or t!e twopubic bones5 tend to t!e $ormation o$ an articulatin% $issure(
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One met!odolo%ic restriction !as to be made: )!ese concepts are valuable onl" in ap!enomenolo%ic and $unctional approac!( )!e" do not tell an"t!in% about t!e conditions a$$ectin%di$$erentiation o$ t!ese tissues and structures( From t!e perspective applied !ere, t!e primar"connective tissue ma" .connect. 3.bind.5 or it ma" .dis#connect. 3.create room.5( .ray/s

Anatomy states t!at . oints in principle are connections between bones 3art!roses5. but t!at t!e.speciali+ed connective tissues o$ t!e constituted oints can be eit!er solid or develop acavit". 345 3p( 4C 5( )!e s"novial oints are called diart!roses( )!e" connect in principle

two enchondral bones 3wit! t!e mandibular and sternoclavicular oints as e2ceptions5( )!e non#s"novial solid oints are called s"nart!roses( Dependin% on t!e properties o$ t!e .intervenin%.connective tissue, t!e latter are $ibrous oints 3sutures, %omp!oses, and t!e s"ndesmoses5 orcartila%inous oints 3s"nc!ondroses5( Fibrous oints are usuall" composed o$ re%ular denseconnective tissue, sometimes o$ somew!at more $ibroelastic connective tissue(

Connection an" Disconnection(Two Ty*es of Fasciae

)!is view o$ two t"pes o$ connectivit" is also applicable to t!e anatom" o$ $asciae( &n %eneral,$asciae in t!e musculoskeletal s"stem e2!ibit two di$$erent mec!anical and $unctional t"pes:

)!ere e2ist muscular $asciae ad acent to spaces t!at are $illed wit! loose areolarconnective tissue 3.slidin% tissue.5 and, sometimes, adipose tissue( )!e" enable t!e slidin% and

%lidin% o$ muscles 3and tendons5 a%ainst eac! ot!er and a%ainst ot!er structures()!ere also e2ist intermuscular and epim"sial $asciae t!at serve as areas o$ insertion $or

nei%!borin% muscle $ibers, w!ic!, in t!is wa", can mec!anicall" reac! a skeletal element via t!ose$asciae wit!out necessaril" bein% attac!ed directl" to t!e bone( 3 5

&n osteopat!ic circles, t!e continuum and continuit" o$ t!e .connective tissue apparatus. in t!e!uman is emp!asi+ed( Suc! a view is in !armon" wit! t!e view described !ere, in particular i$ t!e$ormation o$ cracks and $issures 3.articulatin% spaces.5 as a wa" o$ .connectin%. t!at enablesmobilit" are considered( )!e principal $unction o$ mesoderm as .inner tissue. is .mediatin%. in t!esense o$ .connectin%. 3bindin%5 and .disconnectin%. 3s!apin% space5( )!is multiple $unctionalit" isre$lected in t!e waverin% and diver%ent classi$ications t!at are %iven to connective tissue inte2tbooks o$ anatom" and !istolo%"( For e2ample, .ray/s Anatomy cate%ori+es connective tissuebased on t!e de%ree o$ orientation o$ t!e $ibrous components: irre%ular connective tissue3includin% loose areolar, dense irre%ular, and adipose tissue5 and re%ular 3dense5 connective

tissue 34 5 3p( 645( Wit!in t!e $irst cate%or", areolar 3.loose.5 connective tissue .!olds. or%ans andepit!elia .in place. and !as a variet" o$ $ibers, includin% colla%en and elastin( Re%ular denseconnective tissue, on t!e ot!er !and, $orms li%aments and tendons( Elsew!ere, t!e bookdiscriminates ordinar" 3.%eneral.5 t"pes o$ connective tissue, special skeletal t"pes 3bone andcartila%e5, and !emol"mp!oid tissue as a t!ird cate%or" 34 5 3p( 6>5( )!e $irst two in t!is cate%or"are classi$ied as .supportive connective tissue.; bone 3osseous tissue5 makes up virtuall" t!eentire skeleton in adult vertebrates, and in most ot!er vertebrates, cartila%e is $ound primaril" in

oints, w!ere it provides cus!ionin%(

)!e usual classi$ications o$ connective tissue, includin% $asciae, not based upon $unctional criteriaare not ver" consistent in t!eir cate%ories( .ray/s Anatomy de$ines $asciae as .masses o$connective tissue lar%e enou%! to be visible wit! t!e unaided e"e. 34 5 3p( 675( *s e2amples o$$ascia, t!e s!eat!s around nerves and vessels are mentioned, as are t!e $asciae .on t!e sur$ace.o$ muscles and or%ans and between movable muscles, meant as .mec!anical isolation(. .ray/s

Anatomy makes special re$erence to t!e superficial fascia and to t!e deep fascia, t!e latter inparticular developed in limbs w!ere it condenses to t!icker nonelastic s!eat!s and cases aroundt!e muscles( )!e discrete anatomic structure 3$or instance, muscle5 is considered as re$erence,and t!ere$ore t!e $ascia is de$ined as a kind o$ secondar" au2iliar" envelope to t!at 3primar"5structure( )!is view o$ $asciae as a kind o$ secondar" structure actuall" results $rom t!e scalpel o$anatomists, w!o, w!ile cleanin% muscles $rom t!e $ascial la"ers, !ave disrupted anatomiccontinuit" w!ere it e2ists in vivo(

CONNECTI+E TISSUE IN THEMUSCULOS,ELETAL S-STEM. T/OFUNCTIONAL APPEARANCES
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Not Only Anatomy 0$t Also A!c#itect$!e

&n principle, onl" two kinds o$ $orces !ave to be transmitted over s"novial oints between t!earticulatin% elements in t!e locomotor apparatus: $orces o$ compression and o$ tension(0ompression $orces between t!e articulatin% elements are transmitted via t!e articular sur$aces o$t!e ad acent bone elements( )!e tractive $orces and mec!anical stresses over t!e s"novial ointsare assumed to be transmitted bot! b" passive and b" active components in t!e musculoskeletals"stem( Re%ular dense connective tissue structures suc! as li%aments conve" 3transmit5 t!ose$orces .passivel"(.

From !ere on, t!e term .connective tissue,. i$ not indicated ot!erwise, is used in t!e narrowmeanin% o$ .re%ular dense 3colla%enous5 connective tissue. 3RD0)5( Suc! structures can transmitonl" in a ver" particular position o$ t!e oint t!at is, w!en t!e" are stretc!ed and loaded( )!at isw!" t!is met!od o$ $orce transmission is called .passive(. 1uscles can transmit $orce in var"in%

oint positions because t!e" can activel" c!an%e and adapt t!eir len%t!( *natomicall", t!e twomain components o$ t!is s"stem t!at is, muscles and li%aments are %enerall" t!ou%!t to beor%ani+ed in parallel 1uscles can control oint stabilit" in t!e w!ole ran%e o$ motion, li%amentsonl" in a particular oint position( )!is means t!at t!e periarticular connective tissue, suc! ascapsules and li%aments, w!ic! also pla" roles in providin% mec!anoreceptive in$ormation to t!ecentral nervous s"stem, can be tri%%ered onl" in a particular oint position t!at is, w!en t!erelevant connective tissue is stretc!ed or loaded(

*natomists o$ t!e ?niversit" 1aastric!t, et!erlands, 3 944 5 started to stud" t!e arc!itecture o$RD0) comple2es in t!e musculoskeletal s"stem bot! %loball" and speci$icall" in t!e cubital re%ion()!e" $ound t!at, in t!e !uman elbow oint, passive conve"ance o$ tensile stresses does not occurt!rou%! capsular li%aments alone( &n a simulation model o$ t!e !uman elbow oint, t!e reaction$orces resultin% $rom t!e $orces o$ t!e biceps and brac!ioradialis muscle activit" and an appliede2ternal load s!owed onl" a small di$$erence between simulations wit! an intact capsule 3includin%li%aments5 and simulations wit! t!e capsule sectioned( 347 5 )!ese and ot!er $indin%s c!allen%ednotions about t!e mec!anical arc!itecture o$ t!e periarticular structures in t!at re%ion and t!eirrole in transmittin% $orces and stresses alon% t!e elbow oint( Our team at t!e ?niversit"1aastric!t t!ere$ore developed a new tec!ni-ue o$ dissection to e2plore t!ese anatomicrelations!ips(

)!e central prere-uisite in t!e .alternative. dissection procedure t!at !as been developed was tomaintain continuit" o$ t!e connective tissue b" a connective tissue sparin# dissectionprocedure( &n t!e dorsolateral antebrac!ial and elbow re%ion, t!e antebrac!ial $ascia 3$asciaantebrac!ii5 was not removed, but was opened b" lon%itudinal incisions parallel to t!e lon% a2is o$t!e super$icial e2tensor muscles underneat!( )!e $ascia was t!en released $rom t!e muscle $iberso$ t!e underl"in% muscles( &n t!e distal t!ird o$ t!e so#called muscle bellies, w!ere t!e muscle$ibers convert to t!e perip!eral tendons o$ t!e muscles, t!is separation $rom underl"in% muscletissue was easil" made 3Fi%( 45( ere, underneat! t!e $ascia, a .%lidin% and slidin%. la"er o$ looseareolar tissue was $ound, similar to tissue in areas o$ tendinous bursae( ere, t!e muscles o$ t!edorsal antebrac!ial re%ion appear as t!e anatomicall" separated structures and entities t!at t!e"are conceptuali+ed to be in anatom" dissections and te2tbooks( )!e connective tissue and $asciainvolved serves as a %lidin% and slidin% t!at is, .disconnectin%. medium(
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FIG. 1 'pening of the antebrachial fascia in the distal forearm re-gion 0ntermuscular loose areolar connectivetissue revealed be-t*een the discrete muscle bellies and tendons Left arm, dorsal side, lateral vie*

owever, in t!e pro2imal !al$ o$ t!e $orearm, t!e situation is ver" di$$erent 3Fi%( 75( ere, t!emuscle $ascicles ori%inate $rom t!e antebrac!ial $ascia in an obli-ue or pennate con$i%uration( Onl"a s!arp cuttin% procedure could .remove. t!e $ascia $rom t!e underl"in% muscle $ibers( )!osepro2imal muscle bell" $ibers were also ti%!tl" connected wit! stron% intermuscular connectivetissue la"ers immediatel" continuous wit! $ascia antebrac!ii( So, in t!e pro2imal lateral cubital, t!earc!itecture o$ t!e $ascial connective tissue is -uite di$$erent $rom t!at in t!e distal re%ion: acomple2 apparatus o$ RD0) la"ers is situated on top, between, and deep to t!e muscles( )!ela"ers t!emselves are continuous wit! eac! ot!er, $ormin% walls o$ muscle compartments 3cases5()!e muscle $ibers ori%inate in an obli-ue or pennate con$i%uration $rom t!ose compartment walls;t!e walls, in t!eir turn, conver%e toward t!e lateral !umeral epicond"le( &n $act, an epicondylarconnective tissue apparatus serves as t!e insertion area $or t!e nei%!borin% muscle $ibers( )ensile$orces are t!ere$ore transmitted $rom t!e muscle $ibers to t!e lateral !umeral epicond"le via t!eseconver%in% la"ers o$ RD0)( o muscle $iber inserts directl" to t!e epicond"le( Onl" t!e mostsuper$icial part o$ t!e e2tensor carpi radialis muscle ori%inates $rom t!e supracond"lar !umeralperiosteum( &n addition, in t!e pro2imal lateral cubital re%ion, colla%enous $ibers do not run $rombone to bone as is usuall" t!ou%!t( 1ost o$ t!e colla%enous $ibers in t!e pro2imal lateral cubitalre%ion appear to be interposed between skeletal tissue and muscle $ascicles( )!ere$ore noseparate entit" suc! as a collateral radial ligament could be demonstrated(

F(2' 3 ( )!e compartment walls o$ t!e pro2imal muscle compartment o$ t!e t!ird e2tensor di%itorum muscle areopened and separated $rom t!e muscle $ibers(


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&n a .re%ular. dissection procedure, t!e ne2t step is t!at t!e muscles are dissected and takenout( )!e scalpel !as to cut s!arpl" awa" t!e pro2imal muscle bellies o$ t!e e2tensor muscles, int!is wa" leavin# in situ stron% bands o$ colla%enous connective tissue t!at could be identi$ied ascollateral radial li%ament( &n t!e connective#tissue sparin% dissection, t!e muscle $ibers areremoved and t!e alread"#mentioned epicond"lar connective tissue apparatus is revealed( )!eRD0) strands t!at are usuall" identi$ied as collateral li%ament are indeed an inte%ral part o$ t!eepicond"lar connective tissue apparatus, meanin% t!at, in re%ular dissection, t!e collateral radial

li%ament is dissected out as an arti$actG )!is is demonstrated in Fi%s( and 6(

F(2' 4 ( Hro2imal lateral elbow re%ion( 1uscles are dissected awa" $rom t!e epicond"lar connective tissueapparatus and re$lected 3to t!e le$t5( )!e conver%ence o$ t!e remainin% connective tissue muscle compartment

walls toward t!e lateral !umeral epicond"le is clearl" demonstrated(


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F(2' 5 ( Hro2imal lateral $orearm re%ion( 1uscles and muscular tis#sue !ave been removed( )!e most pro2imale2tensions o$ t!e muscle compartment walls 3t!e epicond"lar connective tissue apparatus5 are le$t in situ,

demonstratin% t!e muscle compartments conver%in% to t!e lateral epicond"le(


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FIG. 5 1a2 !he &classical& in#parallel organi(ation of the iu3taarticular tissue From inside to outside% articular capsule 1blue24 reinforcing iu3ta-articular regular dense connective tissue structures 1ligaments2 1yello*24 and

on the outer side, periarticular muscle 1red2 1b2 !he &classical& organi(ation principle of iu3ta-articular connective tissue running from bone to bone, organi(ed in parallel to the muscular component 1tendons2 'nly

in a particular 5oint position can the connective tissue transmit forces or signal in the sense of mechanoreceptor triggering 16666 versus 77772

&n an in-series con$i%uration as alternativel" described !ere, t!e conve"in% o$ tensile stresses b"t!e colla%enous $ibers also depends on t!e muscle $ascicles t!at are active( &n vivo displacement o$ bones and muscular activit" in$luence t!e state o$ stress and tension o$ connective tissueelements( &n t!is model, passive and active oint#stabili+in% structures or%ani+ed in parallel t!atis, muscles and li%aments wit! mutuall" independent $unctions cannot be distin%uis!ed( )!e ointcapsule and its rein$orcements no lon%er !ave an e2clusive role in t!e passive conve"in% o$ tensilestresses( )!e $unctional units involved in t!e transmission o$ $orces do not consist o$topo%rap!icall" de$ined and separate entities o$ either muscular or li%amentous tissue(

For instance, a structure suc! as t!e supinator aponeurosis ma" be classi$ied as epim"sial $ascia,but also as an aponeurosis or even as a .li%ament. wit! ad ustable len%t! and tension: a.d"nament. 3discussed in more detail s!ortl"5( )!e traditional topo%rap!ic approac! to t!elocomotor apparatus also assumes t!at t!e passive components 3li%aments5 are deep to t!esuper$icial components 3muscles5 t!at are activel" involved in t!e maintenance o$ oint stabilit"and inte%rit" IFi%( =3a,b5J( )!is concept is c!allen%ed b" t!e in.series arc!itecture described !ere(&n t!e lateral cubital re%ion o$ !umans and rats, no li%aments can be distin%uis!ed as separate

entities( )!ere is one oint stabilit" s"stem, in w!ic! muscular tissue and RD0) interweave and$unction mainl" in an in series situation as s!own in Fi%( >3a,b5( )!us, in vivo, t!e periarticular


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connective tissue is loaded and stretc!ed bot! b" t!e movement o$ related skeletal parts and b"t!e tension o$ t!e muscle tissue insertin% to t!is connective tissue(

FIG. 6 1a2 !he alternative in#series organi(ation of the iu3ta-articular tissue From inside to outside% articular capsule 1blue24 periarticular regular dense connective tissue 1yello*2 in series *ith periarticular muscle 1red2

1b2 !he alternative organi(ation of iu3taarticular connective tissue organi(ed in series to the muscular component 0n all 5oint positions the connective tissue of the 5oint is brought to tension and is capable of

transmitting forces and signaling in the sense of mechanoreceptor triggering 16666 and 66662

)!is connective tissue arc!itecture can be better appreciated i$, rat!er t!an talkin% in terms o$collateral li%aments, a .lateral cubital $orce transmission s"stem. 3


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Detailed studies o$ t!e lateral cubital re%ion o$ t!e rat 3discussed later in t!is article5 s!owed t!isarc!itecture( 34C 5 1ost deep and super$icial RD0) la"ers 3as muscle compartment walls5 areor%ani+ed in series wit! muscle $ascicles( 0olla%enous $ibers runnin% $rom bone to bone t!ou%!tto be stressed passivel" b" displacement o$ t!e articulatin% bones !ardl" occur( &nstead, t!ereoccur broad aponeurotic la"ers o$ RD0) to w!ic! relativel" s!ort muscle $ascicles insert, w!ic!, ont!e opposite side, are directl" attac!ed to skeletal elements( Suc! con$i%urations o$ muscle$ascicles attac!ed to t!e periosteum o$ one articulatin% bone and via a la"er o$ RD0) indirectl"

attac!ed to anot!er articulatin% bone, could be considered .d"namic li%aments(. Suc!.d"naments. are not necessaril" situated directl" beside t!e oint cavit" or in t!e deep part o$ t!e

oint re%ion(

/" describin% t!e d"nament as an arc!itectural unit o$ t!e musculoskeletal s"stem, we mean aunit o$ RD0) connected to t!e periosteum o$ a skeletal element wit! muscle $ascicles inseries attac!ed to it( &n Fi%( A3a5 a d"nament is represented in its most basic appearance: aunipennate muscle between two skeletal elements( * t"pical unipennate $orearm muscle asrepresented in Fi%( A3b5 s!ows t!e common appearance o$ t!e d"nament( &n t!is situation, t!edistal RD0) element is represented b" t!e tendon and is situated intramuscularl"( )!e pro2imalRD0) element is represented b" one o$ t!e muscle compartment walls and issituated e&tra muscularl"(

FIG. 7 1a2 Schematic diagram of the &dynament& as architectural unit A regular dense 1collagenous2connective tissue 1+D8!2 layer 1top, yello*2 *ith inserted muscle portion 1middle, red2 Morphologic substrateof proprioception indicated *ith blue dots 1L8, +87.!', see te3t2 and red stripes 1muscle spindles2 Afferent

nerve indicated 1on top, blac92 ote that the innervation pattern of the muscle-related mechanoreceptorsresembles the innervation pattern of a 5oint capsule 1from outside to inside2 1b2 An unipennate forearm muscle

as typical &dynament & )ro3imal 1top left, light grey2, an +D8! layer 1membrane, aponeurosis, septum, etc 2*ith muscle fascicles attached to it, mostly e3tramuscular 1middle, striated red2 Distal 1bottom right, dar9

grey2, an +D8! layer 1tendon, aponeurosis, etc 2 *ith muscle fascicles 1middle, striated2 attached to it, mostly

intramuscular 0n this basic situation, the muscle component is organi(ed as intermediate bet*een t*o +8D! structures

Distal $orearm e2tensor carpi radialis brevis muscles and e2tensor di%itorum muscles clearl" s!owt!is t"pe o$ $unctional unit IFi%( B3c5J( )!e supinator muscle s!ows a variant con$i%uration, wit!distal connective tissue la"ers t!at are well developed, but wit!out an e2tensive connective tissueapparatus intermediatin% at t!e insertion IFi%( B3b5J( )!e lon% !ead o$ t!e triceps s!ows a similarorientation but in t!e .opposite direction. IFi%( B3d5J, wit! developed connective tissue la"erspro2imall" rat!er t!an distall"( &$ neit!er a .pro2imal. nor a .distal. connective tissue apparatus!as been developed, t!e result is a muscle .wit!out aponeurosis or tendon. $or e2ample, t!edeltoideus muscle IFi%( B3a5J( &$ t!e muscular connectin% and intermediatin% tissue !as completel".disappeared,. a li%ament is t!e conse-uence IFi%( B3e5J(
http://ijtmb.org/index.php/ijtmb/article/view/62/82#ref10http://ijtmb.org/index.php/ijtmb/article/view/62/82#ref10http://ijtmb.org/index.php/ijtmb/article/view/62/82#ref10


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FIG. 8. 1a,b,c,d,e2 )ossible appearances of the &dynament& as architectural unit 0n the middle 1c2, the basic situation :see Fig ;1b2< 'n the left 1b2, muscle tissue pro3imally inserting directly to the s9eletal element

1periosteum2 and distally via tendons 'n the right 1d2, muscle tissue distally inserting directly to the s9eletal element 1periosteum2, pro3imally via septa and aponeuroses 'n the e3treme left 1a2, only muscular fascicles,no intermediating regular dense connective tissue 1+D8!2 structure=a &typical muscle & 'n the e3treme right

1e2, no muscle tissue intermediating, only +D8!=a &typical ligament &

&n $act, li%aments, de$ined as strands o$ RD0) runnin% $rom t!e one skeletal element to t!e ne2t,are an e2ception( )!e" have to $e an e2ception( )!e RD0) !as tissue properties o$ !i%!resistance to loadin%, a !i%! de%ree o$ !"steresis, and little elasticit"; a li%ament as interposedstructure between two mova$le bones can t!ere$ore be constructed onl" i$ t!e distance betweent!e opposite points o$ li%amentous insertion on t!e bones c!an%es ver" little durin% t!e ran%e o$motion o$ t!e oint( )!is re-uires speciali+ed desi%n in t!e con$i%uration o$ t!e bones and t!e oint

3sur$aces5, and t!ere are onl" a $ew e2amples o$ suc! .true. li%aments at oints in t!e bod":cruciate li%aments o$ t!e knee oint or li%amentum apicis dentis in t!e atlantooccipital oint(

O$ course in t!e .classical. $ibrous oints, t!e li%amentous or%ani+ation principle is clearl" present,but in suc! cases, t!is or%ani+ation is consistent wit! t!e wa" suc! oints are $unctionall" loaded(Suc! con$i%urations could t!ere$ore be considered e2tremes to t!e %eneral rule( &t bears repeatin%t!at t!ese p!enomenolo%ic and $unctional considerations do not tell an"t!in% about t!e conditionsin and b" w!ic! t!ose tissues and structures di$$erentiate(

*n arc!itectural approac! to t!e anatom" o$ t!e locomotion s"stem as practiced !ere s!ows t!at$asciae e2!ibit a variet" o$ mec!anical relations!ips wit! nei%!borin% tissue and t!ere$ore ma"pla" -uite di$$erent $unctional roles( Sometimes t!e" act as aponeuroses, sometimes t!e" are%lidin% envelopes buildin% oint#like %lidin% spaces( )!e nomenclature .$ascia. s!ould t!ere$ore beconsidered and reevaluated criticall" in ever" re%ion( )!e .classical. $asciae o$ t!e or%ans and o$

muscles usuall" represent t!e .%lidin% $asciae. t"pe 3a%ain, we consider t!e coelom as a kind o$. oint space.5( 1an" epim"sial muscle $asciae $unction in a similar wa"( owever, a $ascia suc! ast!e $ascia cruris or t!e retinaculum patellae $unctions as an epimuscular aponeurosis(

)o understand t!e mec!anical and $unctional circumstances $or t!e $ascial role in connectin% andconve"in% stresses, it is more important to know t!e architecture o$ t!e connective and muscletissue t!an t!e re%ular anatomical order or topo%rap!"( &n principle, t!is approac! applies to ever"$ascial la"er in t!e !uman bod"( One must know $oth w!ere t!e" are situated 3.anatom".5and ho% t!e" are connectin% and connected 3.arc!itecture.5(

THE ARCHITECTURE OF CONNECTI+E TISSUE AS INSTRUMENTAL FOR PROPRIOCEPTION IN THE LOCOMOTOR APPARATUS

T#e S$0st!ate of P!o*!ioce*tion


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)!e arc!itectural view developed !ere !as implications $or t!e understandin% and interpretation o$t!e spatial or%ani+ation o$ t!e nervous a$$erents, wit! related receptors t!at $orm t!e substrate $orproprioception( W!at kind o$ role does t!e arc!itecture in t!e musculoskeletal s"stem pla" in t!e-ualit" o$ centripetal in$ormation $rom t!e various components and tissues o$ t!e s"stem8

)!e usual distinction between muscle a$$erents and articular a$$erents is implicitl" based on t!eanatomical concept t!at 3peri5articular RD0) structures and muscular tissue structures areor%ani+ed in parallel to eac! ot!er alon% t!e oint( )!is latter concept is t!e one t!at wasc!allen%ed in t!e previous part o$ t!is essa"(

0onnective tissue and $asciae are ric!l" innervated( 3 ,7 5 Fascial la"ers ma" t!us pla" an importantrole in proprioception and nociception( 0onsiderations suc! as .arc!itecture versus anatom"3topo%rap!"5,. mutatis mutandis ma" also appl" $or t!e spatial or%ani+ationo$ mechanoreceptors , t!e morp!olo%ic substrate $or proprioception( )o stud" t!e role and$unction o$ mec!anoreceptors in t!e process o$ proprioception, it ma" be important toknow %here t!e" actuall" are located in suc! re%ions and !ow t!e" are or are not connected wit!t!e relatin% tissue elements( )!e actual spatial or%ani+ation o$ suc! receptors can be betterinterpreted $unctionall" w!en it is known !ow t!eir topo%rap!" is related to t!e arc!itecture o$ t!econnective and muscular tissue(

Hroprioception is t!e process o$ conscious and subconscious sensorin% o$ oint position or motion(Encapsulated or unencapsulated mec!anosensitive sensor" nerve endin%s 3mec!anoreceptors5 andrelated a$$erent neurons provide t!e centripetal in$ormation needed $or t!e control o$ locomotionor $or t!e maintenance o$ posture( &n %eneral, suc! mec!anoreceptors are reported to occur eit!eras muscle receptors or as oint receptors( 1uscle receptors are mec!anoreceptors present in t!emuscles, includin% t!eir au2iliar" structures suc! as tendons, aponeuroses, and $asciae( 1usclespindles and @ol%i tendon or%ans 3@)Os5 are t!e best#known t"pes o$ suc! receptors( 34 5 ointreceptors are considered to be situated in oint capsules and related structures, includin%rein$orcin% li%aments( )!ese receptor t"pes are usuall" ordered accordin% to t!e 3ultra5structure o$ t!e receptor itsel$, p!"siolo%ic $eatures, t"pe o$ a$$erent nerve $iber, and ot!er parameters( 34694A ,a 5

&n t!e traditional view, oint receptors pla" t!e leadin% role in monitorin% oint position ormovement $or statest!esis and kinest!esis; muscle receptors are rele%ated to motor $unctions t!atoperate at a subconscious or re$le2 level 3reviewed b" 1c0loske" 34B 5 and 1att!ews 34 55( owever,t!is concept !as been c!allen%ed b" p!"siolo%" investi%ations su%%estin% t!at muscle spindle

a$$erents can also contribute to !uman kinest!esis( 0linical observations in patients w!o retainedt!eir kinest!esis a$ter complete sur%ical removal or interruption o$ oint capsules 3endoprost!eses5and e2periments t!at tested position#sensin% abilities $ollowin% selective anest!esia o$ ointcapsules in vivo provided $urt!er evidence t!at muscle spindles 3and mec!anoreceptors o$ t!eskin5 also contribute to kinest!esis( 37C97 5 &t is o$ten stated t!at oint receptors react onl" at t!ee2tremes o$ oint position, actin% as .limit detectors.( 376 5 &ndeed, it !as been $ound t!at t!edisc!ar%e o$ articular receptors is limited to positions t!at si%ni$icantl" stress t!e oint capsulepositions in w!ic! t!e capsule and related structures are supposed to be strained passivel"( 34B,7=97B5 Ot!er studies su%%est t!at muscle a$$erents provide t!e substrate o$ mid#or $ull#ran%e receptoractivit" 3or bot!5 present in recordin%s $rom articular nerves( 34B,7>9 4 5 &n t!eir well#known studies,*bra!ams, Ric!mond, and /akker describe in t!e neck re%ion o$ t!e cat a variet" o$ sensor"endin%s in so#called non#articular connective tissue( &n neck proprioception, t!e" su%%estattributin% a more important role o$ mec!anoreception to substrate t!at is not situated directl"wit!in or near oint capsules( 3 79 6 5

1ec!anoreceptors are in $act $ree nerve endin%s 3F Es5, w!et!er or not e-uipped wit! speciali+edend or%ans( )!e main stimulus $or suc! receptors is de$ormation( Lariation e2ists as to t!emicroarc!itecture o$ t!e endin%( On t!e one !and, t!ere e2ists t!e principle o$ lamellae around arelativel" simple nerve endin%( )!is represents t!e principle o$ t!e ball# or bean#s!aped LaterHaccini or pacini$orm corpuscles, o$ten called lamellated corpuscles 3


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F Es 3unencapsulated5 1uscle spindles 3sensor" endin%s wit! encapsulated intra$usal muscle $ibers5 @)Os 3t"pe &&& endin%s, relativel" lar%e 4CC 9 >CC Mm diameter spra"#like

endin%s, wit! !i%! t!res!old and ver" slow#adaptin%5

)!e mec!anoreceptors t"picall" associated wit! oints are t!ese:

F Es 3unencapsulated5


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)!e demonstrated substrate o$ proprioception also caused trouble as to morp!olo%ic classi$ication()!e t"polo%" and spectrum o$ nerve $ascicles and nerve terminals $ound !ere e2!ibit $eaturesusuall" associated wit! tendons as well as wit! oint capsules and li%aments(

Summari+in%, t!en, we !ave encountered

an .e2ternal. pat!wa" $or t!e a$$erent nerve $ibers Isee also Fi%( A3a5J( t!e presence o$ %roups &&& and &L nerve $ibers( t!e presence o$ nociceptive, but also putativel" mec!anoreceptive F Es( t!e occurrence o$ .Ru$$ini#like. or .@)O#like. corpuscles at t!e transitional +one between

colla%enous connective tissue la"ers and insertin% muscle $ascicles 3receptors t!at e2!ibit $eaturest!at could lead to classi$ication as @)Os5(

t!e occurrence o$


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FIG. 9 1a2 !he spatial distribution of muscle spindles in the superficial lateral forearm muscle in the rat !hedistribution is clearly more related to the architecture of the pro3imal epicondylar connective tissue apparatusthan to the topography of the muscles !he spindles are presented as thin blac9 lines !he thic9er lines in the

diagram represent the intermuscular septa that are part of the pro3imal regular dense connective tissue1+D8!2 apparatus 1blue, on the left2 and the distal tendons of the superficial e3tensor muscles 1red, on the

right2 1b2 !ypical cross-sections of a rat forearm 1four pro3imal sections from a total of si3 forearm sections2!he muscle spindles and .olgi tendon organs 1.!'s2 in a given segment are pro5ected onto each section in asummative pro5ection Dots are muscle spindles, stars are .!'s ote that .!'s are not only present near or

at distal tendons, the pro3imal intermuscular septa and fasciae also have .!'s arranged to it

P!o*!ioce*tion(Not Only a Matte! of Anatomy 0$t Also of A!c#itect$!e

We !ave demonstrated t!at muscle spindles and @)Os occur in muscular tissue areas inseries wit! RD0) structures( Suc! an area does not o$ten coincide wit! a morp!olo%ic muscle

entit"( )!e arc!itectural relation between t!e RD0) structures seems to de$ine t!e spatialdistribution o$ spindles and @)Os in t!e re%ion as a w!ole( We identi$ied 3sub5units o$ musculartissue in series wit! RD0), so#called muscle spindleN@)O +ones, wit! a relativel" !i%! densit" o$


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mec!anoreceptors( )!e patterns o$ distribution and orientation in suc! +ones are understandable$rom t!e perspective o$ t!e arc!itecture o$ t!e muscular tissue related to t!e connective tissuearc!itecture(

1uscle spindles and @)Os are concentrated mostl" in areas o$ muscular tissue directl"intermediatin% distal and pro2imal RD0) structures t!at is, tendons distall", compartment wallspro2imall"( &$ distal and pro2imal RD0) structures are situated at a relativel" lar%e distance $romeac! ot!er, t!e receptors accordin%l" $orm small elon%ated +ones se%re%ated $rom surroundin%e2tra$usal $ibers 3see Fi%( 4C, patterns 4 and 75( &$ t!e distance between distal and pro2imal RD0)structures is relativel" s!ort, bot! structures are situated more in parallel wit! eac! ot!er: t!espindles run obli-uel" in parallel to eac! ot!er in a relativel" broad muscular area brid%in% a s!ortdistance( (ndividual @)Os occur in a direct one#to#one relation to individual spindles in arelativel" broad area o$ muscleNconnective tissue transition( )!e e2tra$usal $ibers are more or lesse-uall" distributed between t!em 3see Fi%( 4C, patterns and 65( 1uscle portions t!at do not linktwo RD0) structures, but t!at attac! directl" to periosteal tissue, tend to be devoid o$ musclespindles(

FIG. 10 !ypical patterns for muscle spindle>.olgi tendon organ moni-tor (ones 1see te3t2 !he configurationas sho*n at ? 1right2 repre-sents the typical pattern of a @dynament :See also Fig ;1a2 are used courtes" o$t!e Department o$ *natom" and Embr"olo%", ?niversit" o$ 1aastric!t, )!e et!erlands(

CONFLICT OF INTERESTNOTIFICATION)!e aut!or declares t!at t!ere are no con$licts o$ interest(

COP-RIGHTHublis!ed under t!e 0reative0ommons *ttribution on0ommercial# oDerivs (C


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" Freeman 1*, W"ke /( )!e innervation o$ t!e knee oint( *n anatomical and !istolo%icalstud" in t!e cat( Anat 4 >A;4C43Ht 5:=C=9= 7(

"G Freeman 1*, W"ke /( *rticular re$le2es at t!e ankle oint: an electrom"o%rap!ic stud" o$normal and abnormal in$luences o$ ankle# oint mec!anoreceptors upon re$le2 activit" int!e le% muscles( Br Surg 4 >A;=63475: C94CC4(

"; O'0onnor / 9 A4(Ferrell WR( Disc!ar%e c!aracteristics o$ oint receptors in relation to t!eir proprioceptiverole( &n: nik H, ed( Mechanoreceptors% Development, Structure, and Function ew York:Hlenum Hress; 4 BB(

" Rossi *, @ri%% H( 0!aracteristics o$ !ip oint mec!anoreceptors in t!e cat( europhysiol 4 B7;6A3>5:4C7 94C67(

C Ric!mond F , *bra!ams L0( W!at are t!e proprioceptors o$ t!e neck8 )rog Brain+es 4 A ;=C:76=97=6(Ric!mond F , /akker D*( *natomical or%ani+ation and sensor" receptor content o$ so$ttissues surroundin% upper cervical vertebrae in t!e cat( europhysiol 4 B7;6B345:6 9>4(

? *bra!ams L0( eck muscle proprioception and motor control( &n: @arlick D,ed( )roprioception, )osture and Emotion Kensin%ton, *ustralia: ?niversit" o$ ew Sout!Wales, 0ommittee in Host%raduate 1edical Education; 4 B7: 4C 947C(En%lis! *W, 6345:>A9AA(

Q

; En%lis! *W, Weeks O&( 0ompartmentali+ation o$ sin%le muscle units in cat lateral%astrocnemius( E3p Brain +es 4 B6;=>375: >49 >B(

$ En%lis! *W( (

? Holacek H( Receptors o$ t!e oints( )!eir structure, variabilit" and classi$ication( Acta FacMed Univ Brun 4 >>;7 : 94CA(


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?? alata , /adalamente 1*, Dee R, Hropper 1( ?ltrastructure o$ sensor" nerve endin%s inmonke" 3 Macaca fascicularis 5 knee oint capsule( 'rthop +es 4 B6;7375:4> 94A>(

? alata , Retti% ), Sc!ul+e W( )!e ultrastructure o$ sensor" nerve endin%s in t!e !umanknee oint capsule( Anat Embryol 1Berl2 4 B=;4A73 5:7>=97A=(

?G *ndres K , von DPrin% 1, 1us+"nski K, Sc!midt RF( erve $ibres and t!eir terminals o$t!e dura mater encep!ali o$ t!e rat( Anat Embryol 1Berl2 4 BA;4A=3 5:7B 9 C4(

?; *ndrew /4>, 1aastric!t >7CC 1D

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The Architecture of the Connective Tissue in the Musculoskeletal System